Hypoxia-induced mitogenic factor (FIZZ1/RELMα) induces endothelial cell apoptosis and subsequent interleukin-4-dependent pulmonary hypertension

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 306, Issue 12, 2014, Pages

  Yamaji Kegan, Kazuyo ^a   Takimoto, Eiki ^a   Zhang, Ailan ^a   Weiner, Noah C ^a   Meuchel, Lucas W ^a   Berger, Alan E ^a   Cheadle, Chris ^a   Johns, Roger A ^a  

^a DEPARTMENT OF PATHOLOGY   (United States)

Author keywords

Endothelial apoptosis; Human resistin; T helper type 2 inflammation

Indexed keywords

ANGIOPOIETIN 2; ENDOTHELIN 1; HYPOXIA INDUCED MITOGENIC FACTOR; INTERLEUKIN 4; PROTEIN; PROTEIN FIZZ1; PROTEIN RELM ALPHA; RECOMBINANT PROTEIN; RESISTIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; HEART RIGHT VENTRICLE FAILURE; IN VITRO STUDY; INFLAMMATION; LUNG ENDOTHELIUM; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY HYPERTENSION; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE; WILD TYPE;

ENDOTHELIAL APOPTOSIS; HUMAN RESISTIN; T-HELPER TYPE 2 INFLAMMATION;

ANIMALS; ANOXIA; APOPTOSIS; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; HYPERTENSION, PULMONARY; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTERLEUKIN-4; LUNG; MALE; MICE; MICE, INBRED C57BL; PNEUMONIA;

EID: 84902655532     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00279.2013     Document Type: Article

References (63)

1. Angelini DJ, Su Q, Kolosova IA, Fan C, Skinner JT, Yamaji-Kegan K, Collector M, Sharkis SJ, Johns RA. Hypoxia-induced mitogenic factor (HIMF/FIZZ1/RELM alpha) recruits bone marrow-derived cells to the murine pulmonary vasculature. PloS one 5: e11251, 2010.
2. Angelini DJ, Su Q, Yamaji-Kegan K, Fan C, Skinner JT, Champion HC, Crow MT, Johns RA. Hypoxia-induced mitogenic factor (HIMF/ FIZZ1/RELMα) induces the vascular and hemodynamic changes of pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 297: L263-L270, 2009.
3. Angelini DJ, Su Q, Yamaji-Kegan K, Fan C, Skinner JT, Poloczek A, El-Haddad H, Cheadle C, Johns RA. Hypoxia-induced mitogenic factor (HIMF/FIZZ1/RELMalpha) in chronic hypoxia-and antigen-mediated pulmonary vascular remodeling (Abstract). Respir Res 14: 1, 2013.
4. Angelini DJ, Su Q, Yamaji-Kegan K, Fan C, Teng X, Hassoun PM, Yang SC, Champion HC, Tuder RM, Johns RA. Resistin-like molecule-beta in scleroderma-associated pulmonary hypertension. Am J Respir Cell Mol Biol 41: 553-561, 2009.
5. Balasubramaniam V, Le Cras TD, Ivy DD, Grover TR, Kinsella JP, Abman SH. Role of platelet-derived growth factor in vascular remodeling during pulmonary hypertension in the ovine fetus. Am J Physiol Lung Cell Mol Physiol 284: L826-L833, 2003.
6. Chemaly ER, Hadri L, Zhang S, Kim M, Kohlbrenner E, Sheng J, Liang L, Chen J, PKR, Hajjar RJ, Lebeche D. Long-term in vivo resistin overexpression induces myocardial dysfunction and remodeling in rats. J Mol Cell Cardiol 51: 144-155, 2011.
7. Daley E, Emson C, Guignabert C, de Waal Malefyt R, Louten J, Kurup VP, Hogaboam C, Taraseviciene-Stewart L, Voelkel NF, Rabinovitch M, Grunig E, Grunig G. Pulmonary arterial remodeling induced by a Th2 immune response. J Exp Med 205: 361-372, 2008.
8. Dasgupta P, Keegan AD. Contribution of alternatively activated macrophages to allergic lung inflammation: a tale of mice and men. J Innate Immun 4: 478-488, 2012.
9. Davis S, Aldrich TH, Jones PF, Acheson A, Compton DL, Jain V, Ryan TE, Bruno J, Radziejewski C, Maisonpierre PC, Yancopoulos GD. Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning. Cell 87: 1161-1169, 1996.
10. Doherty TA, Khorram N, Sugimoto K, Sheppard D, Rosenthal P, Cho JY, Pham A, Miller M, Croft M, Broide DH. Alternaria induces STAT6-dependent acute airway eosinophilia and epithelial FIZZ1 expression that promotes airway fibrosis and epithelial thickness. J Immunol 188: 2622-2629, 2012.
11. Dorfmuller P, Zarka V, Durand-Gasselin I, Monti G, Balabanian K, Garcia G, Capron F, Coulomb-Lhermine A, Marfaing-Koka A, Simonneau G, Emilie D, Humbert M. Chemokine RANTES in severe pulmonary arterial hypertension. Am J Respir Crit Care Med 165: 534-539, 2002.
12. Eddahibi S, Guignabert C, Barlier-Mur AM, Dewachter L, Fadel E, Dartevelle P, Humbert M, Simonneau G, Hanoun N, Saurini F, Hamon M, Adnot S. Cross talk between endothelial and smooth muscle cells in pulmonary hypertension: critical role for serotonin-induced smooth muscle hyperplasia. Circulation 113: 1857-1864, 2006.
13. Eleuteri E, Di Stefano A, Tarro Genta F, Vicari C, Gnemmi I, Colombo M, Mezzani A, Giannuzzi P. Stepwise increase of angiopoietin-2 serum levels is related to haemodynamic and functional impairment in stable chronic heart failure. Eur J Cardiovasc Prevention Rehab 18: 607-614, 2011.
14. Eloranta ML, Franck-Larsson K, Lovgren T, Kalamajski S, Ronnblom A, Rubin K, Alm GV, Ronnblom L. Type I interferon system activation and association with disease manifestations in systemic sclerosis. Ann Rheum Dis 69: 1396-1402, 2010.
15. Fiedler U, Augustin HG. Angiopoietins: a link between angiogenesis and inflammation. Trends Immunol 27: 552-558, 2006.
16. Filkova M, Haluzik M, Gay S, Senolt L. The role of resistin as a regulator of inflammation: Implications for various human pathologies. Clin Immunol 133: 157-170, 2009.
17. Geng YJ, Libby P. Evidence for apoptosis in advanced human atheroma. Colocalization with interleukin-1 beta-converting enzyme. Am J Pathol 147: 251-266, 1995.
18. Graham BB, Mentink-Kane MM, El-Haddad H, Purnell S, Zhang L, Zaiman A, Redente EF, Riches DW, Hassoun PM, Bandeira A, Champion HC, Butrous G, Wynn TA, Tuder RM. Schistosomiasisinduced experimental pulmonary hypertension: role of interleukin-13 signaling. Am J Pathol 177: 1549-1561, 2010.
19. Hanahan D. Signaling vascular morphogenesis and maintenance. Science 277: 48-50, 1997.
20. Hattori R, Hamilton KK, Fugate RD, McEver RP, Sims PJ. Stimulated secretion of endothelial von Willebrand factor is accompanied by rapid redistribution to the cell surface of the intracellular granule membrane protein GMP-140. J Biol Chem 264: 7768-7771, 1989.
21. Hol J, Wilhelmsen L, Haraldsen G. The murine IL-8 homologues KC, MIP-2, and LIX are found in endothelial cytoplasmic granules but not in Weibel-Palade bodies. J Leukoc Biol 87: 501-508, 2010.
22. Holcomb IN, Kabakoff RC, Chan B, Baker TW, Gurney A, Henzel W, Nelson C, Lowman HB, Wright BD, Skelton NJ, Frantz GD, Tumas DB, Peale FV Jr, Shelton DL, Hebert CC. FIZZ1, a novel cysteine-rich secreted protein associated with pulmonary inflammation, defines a new gene family. Embo J 19: 4046-4055, 2000.
23. Humbert M, Monti G, Fartoukh M, Magnan A, Brenot F, Rain B, Capron F, Galanaud P, Duroux P, Simonneau G, Emilie D. Plateletderived growth factor expression in primary pulmonary hypertension: comparison of HIV seropositive and HIV seronegative patients. Eur Respir J 11: 554-559, 1998.
24. Jurasz P, Courtman D, Babaie S, Stewart DJ. Role of apoptosis in pulmonary hypertension: from experimental models to clinical trials. Pharmacol Ther 126: 1-8, 2010.
25. Katayose D, Ohe M, Yamauchi K, Ogata M, Shirato K, Fujita H, Shibahara S, Takishima T. Increased expression of PDGF A-and B-chain genes in rat lungs with hypoxic pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 264: L100-L106, 1993.
26. Kolosova IA, Angelini D, Fan C, Skinner J, Cheadle C, Johns RA. Resistin-like molecule alpha stimulates proliferation of mesenchymal stem cells while maintaining their multipotency. Stem Cells Dev 22: 239-247, 2013.
27. Koo HS, Kim KC, Hong YM. Gene expressions of nitric oxide synthase and matrix metalloproteinase-2 in monocrotaline-induced pulmonary hypertension in rats after bosentan treatment. Korean Circ J 41: 83-90, 2011.
28. Kugathasan L, Ray JB, Deng Y, Rezaei E, Dumont DJ, Stewart DJ. The angiopietin-1-Tie2 pathway prevents rather than promotes pulmonary arterial hypertension in transgenic mice. J Exp Med 206: 2221-2234, 2009.
29. Kumpers P, Nickel N, Lukasz A, Golpon H, Westerkamp V, Olsson KM, Jonigk D, Maegel L, Bockmeyer CL, David S, Hoeper MM. Circulating angiopoietins in idiopathic pulmonary arterial hypertension. Eur Heart J 31: 2291-2300, 2010.
30. Kuo MC, Patschan D, Patschan S, Cohen-Gould L, Park HC, Ni J, Addabbo F, Goligorsky MS. Ischemia-induced exocytosis of Weibel-Palade bodies mobilizes stem cells. J Am Soc Nephrol 19: 2321-2330, 2008.
31. Lee YW, Kuhn H, Hennig B, Toborek M. IL-4 induces apoptosis of endothelial cells through the caspase-3-dependent pathway. FEBS Lett 485: 122-126, 2000.
32. Lepetit H, Eddahibi S, Fadel E, Frisdal E, Munaut C, Noel A, Humbert M, Adnot S, D'Ortho MP, Lafuma C. Smooth muscle cell matrix metalloproteinases in idiopathic pulmonary arterial hypertension. Eur Respir J 25: 834-842, 2005.
33. Li M, Riddle SR, Frid MG, El Kasmi KC, McKinsey TA, Sokol RJ, Strassheim D, Meyrick B, Yeager ME, Flockton AR, McKeon BA, Lemon DD, Horn TR, Anwar A, Barajas C, Stenmark KR. Emergence of fibroblasts with a proinflammatory epigenetically altered phenotype in severe hypoxic pulmonary hypertension. J Immunol 187: 2711-2722, 2011.
34. Liu T, Jin H, Ullenbruch M, Hu B, Hashimoto N, Moore B, McKenzie A, Lukacs NW, Phan SH. Regulation of found in inflammatory zone 1 expression in bleomycin-induced lung fibrosis: role of IL-4/IL-13 and mediation via STAT-6. J Immunol 173: 3425-3431, 2004.
35. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T) method. Methods 25: 402-408, 2001.
36. Lopes AA, Barreto AC, Maeda NY, Cicero C, Soares RP, Bydlowski SP, Rich S. Plasma von Willebrand factor as a predictor of survival in pulmonary arterial hypertension associated with congenital heart disease. Braz J Med Biol Res 44: 1269-1275, 2011.
37. Lukasz A, Beutel G, Kumpers P, Denecke A, Westhoff-Bleck M, Schieffer B, Bauersachs J, Kielstein JT, Tutarel O. Angiopoietin-2 in adults with congenital heart disease and heart failure. PloS one 8: e66861, 2013.
38. Mora AL, Torres-Gonzalez E, Rojas M, Corredor C, Ritzenthaler J, Xu J, Roman J, Brigham K, Stecenko A. Activation of alveolar macrophages via the alternative pathway in herpesvirus-induced lung fibrosis. Am J Respir Cell Mol Biol 35: 466-473, 2006.
39. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8: 958-969, 2008.
40. Nair MG, Guild KJ, Artis D. Novel effector molecules in type 2 inflammation: lessons drawn from helminth infection and allergy. J Immunol 177: 1393-1399, 2006.
41. Neilson AP, Djuric Z, Land S, Kato I. Plasma levels of resistin-like molecule beta in humans. Cancer Epidemiol 35: 485-489, 2011.
42. Nicolls MR, Taraseviciene-Stewart L, Rai PR, Badesch DB, Voelkel NF. Autoimmunity and pulmonary hypertension: a perspective. Eur Respir J 26: 1110-1118, 2005.
43. Park SH, Chen WC, Hoffman C, Marsh LM, West J, Grunig G. Modification of hemodynamic and immune responses to exposure with a weak antigen by the expression of a hypomorphic BMPR2 gene. PloS one 8: e55180, 2013.
44. Patel L, Buckels AC, Kinghorn IJ, Murdock PR, Holbrook JD, Plumpton C, Macphee CH, Smith SA. Resistin is expressed in human macrophages and directly regulated by PPAR gamma activators. Biochem Biophys Res Commun 300: 472-476, 2003.
45. Pendergrass SA, Hayes E, Farina G, Lemaire R, Farber HW, Whitfield ML, Lafyatis R. Limited systemic sclerosis patients with pulmonary arterial hypertension show biomarkers of inflammation and vascular injury. PloS one 5: e12106, 2010.
46. Price LC, Wort SJ, Perros F, Dorfmuller P, Huertas A, Montani D, Cohen-Kaminsky S, Humbert M. Inflammation in pulmonary arterial hypertension. Chest 141: 210-221, 2012.
47. Sakao S, Taraseviciene-Stewart L, Wood K, Cool CD, Voelkel NF. Apoptosis of pulmonary microvascular endothelial cells stimulates vascular smooth muscle cell growth. Am J Physiol Lung Cell Mol Physiol 291: L362-L368, 2006.
48. Stenmark KR, Fagan KA, Frid MG. Hypoxia-induced pulmonary vascular remodeling: cellular and molecular mechanisms. Circ Res 99: 675-691, 2006.
49. Stewart DJ, Levy RD, Cernacek P, Langleben D. Increased plasma endothelin-1 in pulmonary hypertension: marker or mediator of disease? Ann Int Med 114: 464-469, 1991.
50. Takimoto E, Champion HC, Li M, Belardi D, Ren S, Rodriguez ER, Bedja D, Gabrielson KL, Wang Y, Kass DA. Chronic inhibition of cyclic GMP phosphodiesterase 5A prevents and reverses cardiac hypertrophy. Nat Med 11: 214-222, 2005.
51. Taraseviciene-Stewart L, Kasahara Y, Alger L, Hirth P, Mc Mahon G, Waltenberger J, Voelkel NF, Tuder RM. Inhibition of the VEGF receptor 2 combined with chronic hypoxia causes cell death-dependent pulmonary endothelial cell proliferation and severe pulmonary hypertension. FASEB J 15: 427-438, 2001.
52. Teng X, Li D, Champion HC, Johns RA. FIZZ1/RELMalpha, a novel hypoxia-induced mitogenic factor in lung with vasoconstrictive and angiogenic properties. Circ Res 92: 1065-1067, 2003.
53. Tibbles LA, Woodgett JR. The stress-activated protein kinase pathways. Cell Mol Life Sci 55: 1230-1254, 1999.
54. Tong Q, Zheng L, Lin L, Li B, Wang D, Li D. Hypoxia-induced mitogenic factor promotes vascular adhesion molecule-1 expression via the PI-3K/Akt-NF-kappaB signaling pathway. Am J Respir Cell Mol Biol 35: 444-456, 2006.
55. Tuder RM, Chacon M, Alger L, Wang J, Taraseviciene-Stewart L, Kasahara Y, Cool CD, Bishop AE, Geraci M, Semenza GL, Yacoub M, Polak JM, Voelkel NF. Expression of angiogenesis-related molecules in plexiform lesions in severe pulmonary hypertension: evidence for a process of disordered angiogenesis. J Pathol 195: 367-374, 2001.
56. Vergadi E, Chang MS, Lee C, Liang OD, Liu X, Fernandez-Gonzalez A, Mitsialis SA, Kourembanas S. Early macrophage recruitment and alternative activation are critical for the later development of hypoxiainduced pulmonary hypertension. Circulation 123: 1986-1995, 2011.
57. Verma S, Li SH, Wang CH, Fedak PW, Li RK, Weisel RD, Mickle DA. Resistin promotes endothelial cell activation: further evidence of adipokine-endothelial interaction. Circulation 108: 736-740, 2003.
58. Wedgwood S, Dettman RW, Black SM. ET-1 stimulates pulmonary arterial smooth muscle cell proliferation via induction of reactive oxygen species. Am J Physiol Lung Cell Mol Physiol 281: L1058-L1067, 2001.
59. Yamaji-Kegan K, Su Q, Angelini DJ, Champion HC, Johns RA. Hypoxia-induced mitogenic factor has proangiogenic and proinflammatory effects in the lung via VEGF and VEGF receptor-2. Am J Physiol Lung Cell Mol Physiol 291: L1159-L1168, 2006.
60. Yamaji-Kegan K, Su Q, Angelini DJ, Johns RA. IL-4 is proangiogenic in the lung under hypoxic conditions. J Immunol 182: 5469-5476, 2009.
61. Yamaji-Kegan K, Su Q, Angelini DJ, Myers AC, Cheadle C, Johns RA. Hypoxia-induced mitogenic factor (HIMF/FIZZ1/RELMalpha) increases lung inflammation and activates pulmonary microvascular endothelial cells via an IL-4-dependent mechanism. J Immunol 185: 5539-5548, 2010.
62. Yamaji K, Sarker KP, Kawahara K, Iino S, Yamakuchi M, Abeyama K, Hashiguchi T, Maruyama I. Anandamide induces apoptosis in human endothelial cells: its regulation system and clinical implications. Thromb Haemostasis 89: 875-884, 2003.
63. Yeager ME, Belchenko DD, Nguyen CM, Colvin KL, Ivy DD, Stenmark KR. Endothelin-1, the unfolded protein response, and persistent inflammation: role of pulmonary artery smooth muscle cells. Am J Respir Cell Mol Biol 46: 14-22, 2012.